Changes in the composition of the auditory bulla in southern Solomon Islands populations of the grey cuscus, Phalanger orientalis breviceps (Marsupialia, Phalangeridae)

The auditory bulla is a much-scrutinized taxonomic character of mammals, which is generally regarded as showing a high degree of structural consistency within higher taxa. Observations of bulla variability in populations of the marsupial Phalanger orientalis from the Solomon Islands demonstrate considerable flexibility in bulla makeup, with variable incorporation of the squamosal into the tympanic floor. Studies of the ontogeny of the bulla in Phalanger show the presence of three ossification centres, including an entotympanic. Squamosal invasion of one of these ossificiation centres is seen as a possible result of inbreeding, arising from the mode of colonization of the Solomon Islands by this species. This suggests that, under certain conditions, considerable morphological plasticity may be induced within the selective constraints of bulla function.     

经豚鼠下鼓道口记录耳蜗电图

豚鼠是听觉机能研究最常应用的动物,在其颅骨的鼓泡上,有一卵圆形的小孔,称为下鼓道口,在此插入电极,可抵鼓岬部,能够很好地记录出耳蜗电图。此方法简便、可靠,不需要打开乳突,是从鼓岬部记录耳蜗电图的一种新途径,在听觉机能研究及生理学实验教学中具有广泛的应用价值。     

Ontogeny and cranial morphology of the tympanic region of the Tupaiidae, with special reference to Ptilocercus

The structure of the tympanic region of the skull of Ptilocercus lowii was studied in an embryo of 30 mm crown-rump length and in 5 osteocrania. As in Tupaia, the anterior wall of the bulla of Ptilocercus is not completed by a tympanic process of the alisphenoid, contrary to earlier reports. Ptilocercus resembles Tupaia in the following derived characters. The ventral wall of the tympanic cavity is formed by a rostral entotympanic and by a caudal tympanic process of the petrosal. The entotympanic develops in primary connection with the tubal cartilage. The tympanic aperture of the auditory tube is bordered by the entotympanic. The ring-shaped tympanicum is covered by the entotympanicum and is aphaneric. The musculus tensor tympani is lacking. Among mammals, these characters can be regarded as synapomorphic for the Tupaiidae, that is, to have been present in the common ancestor of the two subfamilies. From the evidence of the tympanic region, the Tupaiidae, therefore, form a monophyletic group. Besides these synapomorphies, there are remarkable differences between Ptilocercus and Tupaia in the structure of the bulla. In Ptilocercus the bulla is smaller and less pneumatized than in Tupaia. An anterior intrabullar septum, present in Tupaia, is lacking in Ptilocercus. The epitympanic wing of the alisphenoid is smaller in Ptilocercus than in Tupaia. A lateral prefacial commissure of the tegmen tympani is present in Ptilocercus, but absent in Tupaia. The caudal tympanic process of the petrosal is larger in Ptilocercus than in Tupaia. These characters are autapomorphic for the Ptilocercinae and for the Tupaiinae, respectively. They demonstrate that the auditory bulla of Ptilocercus and that of Tupaia have evolved independently to a considerable extent. An early phylogenetic separation of their respective ancestors seems likely. The tympanic region of the skull provides no evidence for close relationships of the tree shrews to the primates or to any other eutherians. The classification of the Tupaiidae in a separate order, Scandentia, is supported.     

The angular process of Monodelphis domestica (Didelphidae, Marsupialia) and its relation to the middle ear: an ontogenetic and evolutionary morphologic study

In most marsupials, the angular process is inflected medially. By using an ontogenetic series of Monodelphis domestica, the development of this characteristic structure has been described. In contrast with the eutherian mammals, in marsupials there is retained a close connection between the dentale and the tympanicum and goniale; it is well known that these 2 elements of the middle ear are derived from the angulare and prearticulare of the reptilian lower jaw. At the neonatal stage, the dentale and tympanicum are both relatively vertically orientated; during the following 2 weeks, they take an increasingly oblique position, which is primarily caused by the rapid growth of the braincase. Only after the eruption of the first teeth, the ascending ramus of the dentale takes a more and more vertical position, whereas the angular process remains with its tip near the medioventral floor of the tympanic bulla. The bulla shows at this place a rectangular fenestra which is covered by a membrane of loose connective tissue; the tip of the angular process, which is always free of muscular insertions, maintains contacts with this fenestra throughout life. During juvenile and adult life stages, the process becomes somewhat removed from the fenestra for obvious reasons, but at a gape of about 40 to 50 degrees it inevitably must touch the "inferior tympanic membrane" and possibly also the tympanic ring. It is speculated that the relationship between the angular process and the tympanic bulla represents a specific form-function complex for sound transmission, which may be a modified retention from archaic mammalian conditions. Further details of the ontogenetic development of the tympanic region have been described which may be of some relevance for the evolutionary morphology of mammals: The tympanic process of the petrosal, which fixes the posterior end of the tympanic ring, is formed by 'Zuwachsknochen' (additional bone) but not by cartilage. The styloid process remains cartilaginous throughout life: its free tip ends in the lateral wall of the tympanic cavity and it is closely connected with the collum mallei and the posterior end of the tympanicum; it guides the chorda tympani and may therefore be homologous with the cartilage of Spence. The cartilage of Paauw is interpreted in terms of functional morphology. A model of evolutionary transformation of the dentale-tympanicum complex in mesozoic mammals in outlined on the basis of the ontogenetic findings in Monodelphis and other didelphid and dasyurid marsupials.     

First Description of the Auditory Region of a Tremarctinae (Ursidae,Mammalia) Bear: The Case of Arctotherium angustidens

Here we present the first detailed morphological study of the auditory region of a tremarctine bear, the South American giant short-faced bear Arctotherium angustidens. We compared 19 specimens of A. angustidens with other tremarctines and ursines. Through the use of CT scans, we confirmed the presence of a recesus epitympanicus and an anterior incomplete septum of uncertain homology, not related with the septum bullae nor with the longitudinal septum formed by the ecto- and the entotympanic. A secondary crus formed by the lateral semicircular canal (LSC) with the posterior semicircular canal (PSC) of the inner ear was observed in A. angustidens, A. bonariense, Tremarctos ornatus, Ursus spelaeus, and Ursus arctos. This secondary crus was not previously reported for ursids. We also observed that the intraspecific variation in the auditory region of A. angustidens is related to 1) the position of the foramen postglenoideum, 2) the anterior projection of the bulla tympanica over the foramen lacerum and over the opening of the Eustachian tube (medial process of the bulla tympanica), and 3) the projection of the bulla tympanica over the posterior surface of the processus postglenoideus (tympanic process). In addition to this variation, we also identified the presence of interspecific variation in the external auditory region among Tremarctinae and Ursidae. These differences are related to the size of the processus mastoideus and the processus paraoccipitalis, the position of the foramen postglenoideum, and the presence/absence of contact between the bulla tympanica and the processus paraoccipitalis.     

Auditory acuity in the orientation behaviour of the bushcricket Pachysagella australis walker (Orthoptera,Tettigoniidae, Saginae)

The female tettigoniid Pachysagella australis (Saginae) orients to the call of the conspecific with an angular acuity of ±5°. This acuity is mediated by sound entering to the tympanic receptors through the auditory trachea and the slits exterior to the tympanic membranes. The phonokinetic response of females was filmed in an arena. The slit system was blocked on both anterior and posterior ports with the effect that the female spiralled towards the sound source; blocking the posterior slit alone reduced the auditory acuity as did the partial occlusion of the fore slit, but in both cases the female located the male. Complete blocking of the auditory spiracle caused the insect to spiral towards the unoperated side, whereas reducing the sound input to one side by some 8–12 dB, by plugging the auditory bulla with compacted cotton wool, did not substantially affect the orientation pattern of the insect. Ablation of the tympanic organ on one side caused the female to move in a circular pattern to the unoperated side. A hypothesis is formulated whereby the female, when actively orienting to the calling male, may use the slit port system to gain a high degree of auditory acuity to sound in front of her body axis. When off target she may use the less accurate spiracular input system. This system, with its greater sensitivity to high frequency sounds, may function as an effective anti-predator warning system.     

Patterns of variation in the tympanic bulla of tuco-tucos (Rodentia,Ctenomyidae, Ctenomys)

As subterranean rodents live in burrows and are constrained by the physics of their environment to vocalize, mainly in low frequencies, their expanded middle ear cavities are associated with enhanced lower-frequency hearing. Previous literature has widely acknowledged inflated tympanic bulla as a character to be found in the majority of the Ctenomys species. To explore the morphology of Ctenomys tympanic bulla, we studied a sample of 669 skulls, obtained from 21 species, for tympanic bulla size, volume, and internal structure. The study determined that bullar inflation does not seem to be the rule in Ctenomys and that the relationship between bullar size (volume) and skull size do not correspond to the phylogeny based on cytochrome b sequences thus probably being a species-specific adaptive characteristic. We also found that the internal bullar structure differs between taxa, depending on the relative contributions of cancellous (alveolar) and septate patterns to the partitioning of the bulla.     

The ontogenesis of the tympanic region of the Procaviidae (Mammalia: Hyracoidea)

Lindahl (1948) has described the early ontogenesis of 14 fetal stages of Procavia capensis. The oldest fetus of his series has had a headlength of 20 mm. It is the series with which the present account on the development of the tympanic region in hyracoids starts. Further middle to late fetuses have been studied by means of serial sections or macroscopic preparations. First 5 different ontogenetic stages are described, and then we follow the development of different organs in their ontogenesis. Results: 1. The development of the tympanic region is almost completed at birth, except for the external meatus. The bulla tympani is fully ossified. 2. The entotympanic forms the medial and rostral part of the Bulla tympani. Its anlage is first met at a headlength of 31 mm. From the very beginning, it is fused with the tubal cartilage. Hyracoids do not have a caudal entotympanic. The cartilaginous mass-taken for a caudal entotympanic by Van der Klaauw (1926)-is actually a tympanic process of the petrosal. Extensive discussion reveals that the structures named entotympanics in some eutherians are most likely not homologous. 3. It is almost impossible to separate the entotympanic from the tympanic in neonates already. This is due to the surprising fact that the tympanic produces secondary cartilage at the suture between the 2 elements. 4. A gonial is lacking in hyracoids; instead the malleus is fixed in a peculiar way at the tympanic. 5. According to Lindahl (1948), the stapedial artery exists till a fetal headlength of 14 mm. Then the artery obliterates but the crura stapedis with the stapedial foramen persist. 6. Hyracoids possess a tympanohyal which changes its relation to the facial nerve during ontogenesis. 7. The development of the Eustachian sac (Diverticulum tubae auditivae) is described and compared with its development in the horse, based on the few data available in literature. 8. The internal carotid artery changes its course during its ontogenesis. Up to late stages it passes over the caudal part of the Eustachian sac and along the medial side of the Bulla tympani. A sulcus caroticus might still be seen in neonates. It is only in postnatal development that it looses the course along the bulla and passes along the mediocaudal side of the Eustachian sac. 9. The formation of the Recessus meatus acustici externi in exactly takes place the way described only once by Hammar (1902). The cavitation of the recessus occurs independently of the cavity of the external meatus.     

Molecular systematics of marsupials based on the rRNA 12S mitochondrial gene: the phylogeny of didelphimorphia and of the living fossil microbiotheriid Dromiciops gliroides thomas

Nucleotide sequence data from the mitochondrial 12S rRNA gene were used to evaluate the phylogenetic relationships among the major groups of didelphimorph and paucituberculatan marsupials from South America, the microbiotheriid Dromiciops gliroides, and representatives of four orders of Australasian marsupials. Based on approximately 800 bp in 18 genera, we conclude that the didelphids constitute a monophyletic group with large-sized forms differentiated from small opossums, while Caluromys constitutes the sister taxon to didelphids. The peramelid Isoodon was recovered as the sister taxon to the paucituberculatans Caenolestes and Rhyncholestes, although it is in an uncertain phylogenetic position within the marsupial tree. Dromiciops was recovered as a well-differentiated lineage from South American opossums within the Australidelphian radiation of metatherians that include dasyurid, diprotodontian, and notoryctemorph marsupials.     

Molecular Systematics of Marsupials Based on the rRNA 12S Mitochondrial Gene: The Phylogeny of Didelphimorphia and of the Living Fossil Microbiotheriid Dromiciops gliroides Thomas

Nucleotide sequence data from the mitochondrial 12S rRNA gene were used to evaluate the phylogenetic relationships among the major groups of didelphimorph and paucituberculatan marsupials from South America, the microbiotheriid Dromiciops gliroides, and representatives of four orders of Australasian marsupials. Based on approximately 800 bp in 18 genera, we conclude that the didelphids constitute a monophyletic group with large-sized forms differentiated from small opossums, while Caluromys constitutes the sister taxon to didelphids. The peramelid Isoodon was recovered as the sister taxon to the paucituberculatans Caenolestes and Rhyncholestes, although it is in an uncertain phylogenetic position within the marsupial tree. Dromiciops was recovered as a well-differentiated lineage from South American opossums within the Australidelphian radiation of metatherians that include dasyurid, diprotodontian, and notoryctemorph marsupials.     

The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole.

Alternative hypotheses in higher-level marsupial systematics have different implications for marsupial origins, character evolution, and biogeography. Resolving the position of the South American monito del monte (Order Microbiotheria) is of particular importance in that alternate hypotheses posit sister-group relationships between microbiotheres and taxa with disparate temporal and geographic distributions: pediomyids; didelphids; dasyuromorphians; diprotodontians; all other australidelphians; and all other marsupials. Among Australasian marsupials, the placement of bandicoots is critical; competing views associate bandicoots with particular Australasian taxa (diprotodontians, dasyuromorphians) or outside of a clade that includes all other Australasian forms and microbiotheres. Affinities of the marsupial mole are also unclear. The mole is placed in its own order (Notoryctemorphia) and sister-group relationships have been postulated between it and each of the other Australasian orders. We investigated relationships among marsupial orders by using a data set that included mitochondrial and nuclear genes. Phylogenetic analyses provide support for the association of microbiotheres with Australasian marsupials and an association of the marsupial mole with dasyuromorphs. Statistical tests reject the association of diprotodontians and bandicoots together as well as the monophyly of Australasian marsupials. The origin of the paraphyletic Australasian marsupial fauna may be accounted for by (i) multiple entries of australidelphians into Australia or (ii) bidirectional dispersal of australidelphians between Antarctica and Australia.     

Auditory development in the mouse: Structural maturation of the middle ear

The development of middle-ear structures in the mouse was examined in nine groups of pups between 1 and 45 days of age. The area of the tympanic membrane (pars tensa and pars flaccida), the length of the lever arms of the malleus and incus, the surface area of the oval window, and the volume of the bulla all showed systematic changes during neonatal life. The area of the oval window reached maturity first and the lever arms achieved 90% of their adult size on day 11. The tympanic membrane achieved the same criterion on day 18. These data help us further to understand the processes that contribute to the functional ontogeny of the middle ear.     

From Problem Taxa to Problem Solver: A New Miocene Family,Tranatocetidae, Brings Perspective on Baleen Whale Evolution

Miocene baleen whales were highly diverse and included tens of genera. However, their taxonomy and phylogeny, as well as relationships with living whales, are still a subject of controversy. Here, “Mesocetus” argillarius, a poorly known specimen from Denmark, is redescribed with a focus on the cranial anatomy. It was found to represent not only a new genus, Tranatocetus gen. nov., but also a new family; Tranatocetidae. The whales of this family have the rostral bones either overriding or dividing the frontals; the rostral bones are contacting the parietals and nasals dividing the maxillae on the vertex; the occipital shield is dorsoventrally bent. The tympanic bulla is particularly characteristic of this family featuring a short, narrow anterior portion with a rounded or squared anterior end and a wider and higher posterior portion that is swollen in the posteroventral area. A phylogenetic analysis including 51 taxa supports a monophyletic group comprising most Neogene and modern whales, with Tranatocetidae being possibly closer related to Balaenopteridae (rorquals) than to Cetotheriidae. Tranatocetidae exhibit a charahteristic bulla shape. In fact, all Neogene and modern mysticete families examined have a unique shape of the tympanic bulla that is diagnostic at family-level. Inclusion of problematic taxa like Tranatocetus argillarius in phylogenies brings new understanding of the distribution and diagnostic value of character traits. This underlines the need for re-examination of earlier described specimens in the light of the wealth of new information published in later years.     

中国穿山甲和马来穿山甲头骨量度的测定及比较

全球共有7种穿山甲。本文报道的是中国穿山甲和马来穿山甲的头骨形态学资料,涉及头骨特征描述和一些形态学指标测定。被测定的指标主要有颅全长、基底长、腭长、眶间宽、后头宽、鼻骨长、鼻骨宽、脑颅高、听泡长和下颌长,并且在这两个物种之间进行了比较。结果表明,(1)这两个物种头骨形态十分相似,但马来穿山甲头骨细长,听泡长小于10mm(n=12),鼻骨狭长,前后部宽窄相似,两鼻骨外侧缘内凹或平行,鼻骨宽长之比值小于0 3000(0 2025～0 2811,n=12);而中国穿山甲头骨较粗短,听泡长大于11mm(n=46),鼻骨宽短,后部较前端宽,外侧缘外凸,鼻骨宽长之比值大于0 3000(0 3154～0 5325,n=33)。这些异同之处,可以作为区分这两个物种的依据。(2)中国穿山甲华南亚种与海南亚种头骨各变量之间的差异不显著(P>0 05),用颅全长是否大于83mm来区分这两个亚种不能成立,但海南亚种头骨上颌骨的颧突和鳞骨的颧突通常越过眶颞窝完全相接触,如果不是这样,则在它们之间有一个小的骨质棒状结构将它们连接起来。     

The correlation of the size of the pinna and the auditory bulla in specialized desert rodents

Relation between size of pinna and auditory bulla in specialized desert rodents (families Allactagidae, Dipodidae, Gerbillidae, Heteromyidae, and genus Selevinia) is statistically significant and described by hyperbola. The empirical distribution of respective sizes can be interpreted as a total of two main trends. One is enlargement of the pinna, the bulla remains small (most of Allactagidae), another is enlargement of the bulla, the pinna remains small (Gerbillidae, Heteromyidae, Selevinia, most Dipodidae). A few species display moderate enlargement of both pinna and bulla, while in Euchoreutes they both are hypertrophied. Biomechanical preconditions are supposed to be following. Enlargement of the pinna is responsible for increasing of both sensitivity and locatory abilities of the hearing organ, while enlargement of the bulla is responsible for the first function only. So, the two main trends are results of selection of development of the hearing organ at the level of either pinna or bulla. It is shown by dispersion and correlation analyses that size of the parts of the hearing organ under investigation are correlated mostly with mobility and escaping mode. It is concluded therefore that the rodents characterized by active and speedy escaping from predation display the first of the above trends, while the rodents characterized by passive escaping from predation display the second trend.     

Scaling of the marsupial middle ear and its functional significance

The marsupial middle ear performs an anatomical impedance matching for acoustic energy travelling in air to reach the cochlea. The size of the middle ear sets constraints for the frequencies transmitted. For generalized placental mammals, it has been shown that the limit for high-frequency hearing can be predicted on the basis of middle ear ossicle mass, provided that the ears fulfil requirements of isometry. We studied the interspecific size variation of the middle ear in 23 marsupial species, with the following measurable parameters: skull mass, condylobasal length, ossicular masses for malleus, incus and stapes, tympanic membrane area, oval window area, and lever arm lengths for malleus and incus. Our results show that the middle ear size grows with negative allometry in relation to body size and that the internal proportions of the marsupial middle ear are largely isometric. This resembles the situation in placental mammals and allows us to use their isometric middle ear model to predict the high-frequency hearing limit for marsupials. We found that the isometry model predicts the high-frequency hearing limit for different marsupials well, indicating that marsupials can be used as auditory models for general therian mammalian hearing. At very high frequencies, other factors, such as the inner ear, seem to constrain mammalian hearing.     

The ear region of the marsupial sabertooth,Thylacosmilus: Influence of the sabertooth lifestyle upon it,and convergence with placental sabertooths

The mastoid auditory bulla of the extinct marsupial sabertooth, Thylacosmilus, has an enlarged, complex hypotympanic sinus but lacks an alisphenoid contribution. These are marked departures from the usual marsupial condition. Details of the ear region of Thylacosmilus are compared with those of the convergent, extinct placental sabertooth, Smilodon, and each is compared with less specialized related forms to define differences and similarities of the evolutionary paths that led to the striking overall convergence. Functional factors such as pressure transformer ratio (PTR), impedance transformer ratio (ITR), acoustic impedence at the eardrum, and the fraction of the sound energy theoretically transmitted to the inner ear cannot be estimated for Thylacosmilus because certain critical measures are still unknown (tympanum size, ossicle lever arm ratios). However, in both sabertooths enlarged complex hypotympanic sinuses, characterized by expansions and contractions, are greatly developed. They vastly increase middle ear space (volume) and must have influenced these factors. In both, the sinuses provide the large air volume needed to prevent excessive damping of sound energy transmission (Hunt and Korth, '80), and both are believed to have achieved a further modulation of the system from the cushioning or “pillow” effect of the confined air as it directly damps the tympanum itself. Thylacosmilus has still another feature that may have given greater control over damping of sound energy transmission: the direct opening (probably membrane covered) of one of the sinus cavities into the side of the meatal tube. In this feature, as in others noted earlier (Turnbull, '76, '78), we see a greater degree of specialization in this marsupial sabertooth than in a placental counterpart.     

Age estimation in bowhead whales using tympanic bulla histology and baleen isotopes

Tympanic bullae and baleen plates from bowhead whales of the Western Arctic population were examined. Growth layer groups (GLGs) in the involucrum of the tympanic bone were used to estimate age of the whales, and compared to stable isotope signatures along transects of baleen plates and the involucrum. The involucrum of the tympanic bone consists of three regions that form in utero, during nursing in the first year, and during the first decades of life, respectively. Life history events, such as annual migration, are recorded in the bowhead tympanic bulla. It is likely that bone growth in the bowhead tympanic occurs during periods of high food intake, while slow or arrested growth occurs during periods of low food intake. Comparisons between numbers of GLGs in the tympanic, number of isotopic oscillations in a baleen plate, length of the baleen plate, and total whale length show correlation coefficients as high as 0.97. The tympanic GLG method is particularly useful for estimating the age of whales up to 20 yr old.